Int J Ophthalmol, Vol. 13, No. 3, Mar.18, 2020 www.ijo.cn Tel: 8629-82245172 8629-82210956 Email: [email protected]

·Clinical Research· Correlation of the history of and the retinal artery occlusion: a nested case-control study

Yue-Yan Xiao1, Wen-Bin Wei1, Ya-Xing Wang1, Ai-Dong Lu2, Shuo-Hua Chen3, Lu Song3, Shou-Ling Wu3

1Beijing Tongren Eye Center, Beijing Key Laboratory In the case group, 28 patients (62.2%) had a central retinal of Intraocular Tumor Diagnosis and Treatment, Beijing artery occlusion (CRAO), and 17 patients (37.8%) had a Ophthalmology & Visual Sciences Key Lab, Beijing Tongren branch retinal artery occlusion (BRAO). A total of 18 patients Hospital, Capital Medical University, Beijing 100730, China (40.0%) had a stroke before the RAO (mean 4.04±3.88y 2Department of Ophthalmology, Kailuan General Hospital, before the RAO), and 31 patients (81.6%) had infarctions Tangshan 063000, Hebei Province, China or malacia identified by the cranial computed 3Department of Cardiology, Kailuan General Hospital, (CT) scans. The basal ganglia and centrum semiovale Tangshan 063000, Hebei Province, China were the most frequently involved regions. Plaques in the Correspondence to: Wen-Bin Wei. Beijing Tongren Eye common carotid artery were present in 32 patients (88.9%). Center, Beijing Key Laboratory of Intraocular Tumor Conditional multivariate logistic regression analysis showed Diagnosis and Treatment, Beijing Ophthalmology & Visual that the RAO was found to be associated with the history of Sciences Key Lab, Beijing Tongren Hospital, Capital Medical stroke (P=0.0023, OR=28.794; 95%CI: 3.322-249.586). University, Beijing 100730, China. [email protected] ● CONCLUSION: A history of stroke can significantly Received: 2019-11-23 Accepted: 2020-01-08 increase the incidence of RAO. Exists of plaque in the carotid artery is mean more than its severe for RAO. Abstract ● KEYWORDS: retinal artery occlusion; stroke; risk factor; ● AIM: To analyze the systemic factors including stroke embolic source; carotid plaque history related to the retinal artery occlusion (RAO). DOI:10.18240/ijo.2020.03.10 ● METHODS: Patients with an exact diagnosis of RAO in the medical database of the Kailuan Corporation were Citation: Xiao YY, Wei WB, Wang YX, Lu AD, Chen SH, Song L, Wu identified as the case group. Five patients without RAO SL. Correlation of the history of stroke and the retinal artery occlusion: a were added for each case from the Kailuan Study and nested case-control study. Int J Ophthalmol 2020;13(3):431-437 matched for sex and age (age±2) as the control group. The Kailuan Study is a general population-based cohort study INTRODUCTION in northern China, in which a total of 101 510 individuals etinal artery occlusion (RAO) is an emergency in (81 110 men) aged 18-98y were recruited to participate R ophthalmology and can cause severe damage to visual in the study. And the participants were bi-annually re- acuity (VA). The incidence of RAO is below 3.5/100 000[1], examined. The database of both groups was from Kailuan and the prognosis is grave. Furthermore, the lifetime of central study of 2010 cohort. All the information, including the retinal artery occlusion (CRAO) patients is reduced by 10y as demographic characteristics, lifestyle behaviors, medical compared with healthy controls[2]. Its diagnosis is relatively comorbidities, medical history, family medical history, drug definite, according to the sudden visual deterioration history, usage, anthropometric measurements, blood pressure stereoscopic colour and fluorescence measurement, blood sample laboratory assessment, urine fundus (FFA) examination. According to the tests, and other physical examinations were all collected. A pathogeny, researchers divided CRAO into 4 categories: non- retrospective nested case-control method was used for this arteritic CRAO, non-arteritic CRAO with cilioretinal artery study. Conditional multivariate logistic regression was used sparing, arteritic CRAO with giant cell arteritis, branch retinal to analyze the risk factors with SPSS 13.0 software and SAS artery occlusion (BRAO) consists of BRAO and cilioretinal 9.3 software. artery occlusion (CLRAO)[3-4]. ● RESULTS: A total of 45 patients were included as the The embolic source of RAO mainly from carotid arteries and case group, and the control group included 225 patients. aorta. And it can also be caused by running embolic material

431 Stroke and retinal artery occlusion arising in the course of atrial fibrillation or dilated left were administered in person by qualified doctors, in which ventricle, giant cell arteritis, and other autoimmune diseases or information was obtained including demographic and haematological disorders[5-6]. The reported systemic diseases socioeconomic data, education level, average income of each associated with RAO include hypertension, hyperlipidemia, family member, medical history, family medical history, and peripheral vascular disease. Studies confirmed that RAO alcohol consumption, smoking status, dietary data, physical patients associated with an increased risk of stroke, and stroke activity, and sleeping duration and quality. The questionnaires, risk in CRAO patients was 2.7-fold higher as compared anthropometric measurements, blood pressure measurement, with controls, especially the first week after the CRAO blood sample laboratory assessment, urine tests, and other occurrence[7-9]. But whether the stroke history or asymptomatic physical examination findings were all performed by infarction in the head can imply a risk for RAO need to be rigorously trained doctors and nurses and have been described studied. in detail previously[10-12]. The nested case-control study method is usually used to those The “retinal artery occlusion” was searched for in the Kailuan diseases with a low incidence or when the interest of exposure Medical Database for the Kailuan Corporation between 2006 factors difficult to obtain. But this method requires the case and 2015. And then all these patients were needed to be group and the control group from the same cohort to get an checked with the detailed medical records in the hospital where efficient statistical result with low selection bias. This study the patients were diagnosed with the disease. All those patients aimed to investigate the systemic risk factors for RAO in a were needed to meet the inclusion criteria. And those without large population with the nested case-control study to identify detailed medical records or could not meet the inclusion potential subgroups at risk, especially those patients with a criteria been excluded. stroke history, and help to identify potential areas for future Thinking about most people took the carotid ultrasonography study. examination in the 2010 Kailuan Study, we randomly added 5 SBUJECTS AND METHODS people without RAO disease matched by age (age±2) and sex Ethical Approval The study was performed according to the for each patient in the 2010 Kailuan Study to be the control guidelines of the Declaration of Helsinki and was approved group. And all these people had been checked without RAO by the Ethics Committee of Kailuan General Hospital. All the by normal eye examination in the Ophthalmology Department. participants signed a written informed consent form. And all And all the analyses about the demographic and clinical personal information about the participants is fully protected. features in the two groups were based the results in the 2010. Data Sources The study was a retrospective study based on And all these cases in the two groups were followed to 2015. the Kailuan Medical Network, which was connected with the The medical records were checked and recorded all the insurance system and the medical records of all the participants demographic data of case group, including age, sex, lifestyle, of Kailuan Study were added in real-time. The Kialuan study dietary habits, complicated systemic diseases, and drug usage, was a prospective cohort study conducted in the community were recorded. Ophthalmic evaluations included the following: of Kailuan in the industrial city of Tangshan, China. Between VA; intraocular pressure measurement; slit-lamp examination June 2006 and October 2007, a total of 101 510 individuals of the anterior segment, lens, and vitreous; stereoscopic (81 110 men) aged 18-98y were recruited to participate in colour fundus photography; FFA; and visual field testing with the study, and the participants were bi-annually re-examined. an automated perimeter. The results of carotid , The Kailuan Corporation is a large coal mining company in echocardiograms, cranial computed tomography (CT) scans Tangshan city, in the Hebei Province of China. The medical and blood tests were recorded. Body mass index (BMI) was insurance centre has a separate division for this corporation; calculated as follows: BMI (kg/m2)=body weight (kg)/height2 thus, almost all medical information of the employees and (m2). The estimated glomerular filtration rate (eGFR) was retirees can be searched for in this database. The medical calculated with the Chronic Kidney Disease Epidemiology insurance policy in Tangshan is set to provide reimbursements Collaboration (CKD-EPI) equation[13]. Other systemic or for local in-patients only. Most critical patients would be neurologic evaluations were also performed to rule out related hospitalized. And we can search all the patients’ diagnosis, causes of visual loss. names, sex, identity card numbers, and find the hospital for Inclusion Criteria for the Study In line with the RAO where and when the therapy be taken in this database. diagnostic criteria, the diagnosis of RAO was based on the All participants underwent questionnaire assessments, and presence of various classical clinical findings as follows[14]: 1) clinical and laboratory examinations were conducted in the There was a history of a sudden onset of visual deterioration 11 hospitals responsible for the healthcare of this community in the eye. 2) On the initial ophthalmic evaluation, there was in Tangshan every two years since 2006. Questionnaires evidence of acute retinal ischaemia in the distribution of the

432 Int J Ophthalmol, Vol. 13, No. 3, Mar.18, 2020 www.ijo.cn Tel: 8629-82245172 8629-82210956 Email: [email protected] occluded retinal artery. 3) FFA showed evidence of the absence or marked stasis of circulation in the involved branch of the retinal artery, except in eyes with transient RAO. All criteria had to be fulfilled for inclusion in the study. Patients with a detailed systemic disease history and physical examination record were included. RAO associated with temporal arterits was excluded either clinically based on the presence of symptoms and the presence of an elevated erythrocyte sedimentation rate (ESR) or protein C or based on temporal artery biopsy, where possible. Statistical Analysis A retrospective nested case-control analysis was used for this study. SAS 9.3 software was used to Figure 1 The fundus examination of the right eye CRAO with record the information and perform a conditional multivariate cilioretinal artery spring. logistic regression analysis. Statistical analyses were performed Table 1 BRAO-the affected branch with SPSS 13.0 software and SAS software by one researcher Affected branch Cases (%) who was blinded to the disease status of the patients, the Nasalis superior 2 (11.8) medications, the examination findings, and the time sequence. Nasalis inferior 0 All the variables collected in the Kailuan Study were selected Temporalis superior 3 (17.7) to make statistical analysis. At first, the measurement data and Temporalis inferior 10 (58.8) numerical data were statistically analyzed with the t-test or the Cilioretinal artery 2 (11.8) 2 χ test, respectively, to evaluate the demographic and clinical BRAO: Branch retinal artery occlusion. features between the two groups. The conditional multivariate logistic regression analysis was used to analyse the risk evaluation revealed counting fingers VA in 1 patient (5.9%); factors for RAO. A P value <0.05 was considered statistically 6 patients (35.3%) had a VA<0.1 and 10 patients (58.9%) had significant. a VA≥0.1. Three patients (6.7%) among all the RAO patients RESULTS experienced an improvement of 2 lines in VA after undergoing Demographic and Clinical Characteristics Based on eye massage, treatment to decrease the intraocular pressure, the Kailuan Medical Database of the Kailuan Corporation vasodilator medicine intravenous drip, or other therapies between 2006 and 2015, 65 patients were diagnosed with included intravenous fibrinolytic agents, oxygen inhalation, RAO. According to the diagnostic inclusion criteria and oral aspirin, and so on, to improve the microcirculation, in after excluding patients without detailed medical records, 45 which one patient were treated with nitroglycerin before being patients (45 eyes) were included in the analysis. The mean seen by an ophthalmologist. The condition of two patients age was 59.98±10.26y. A total of 39 patients (86.7%) were (4.4%) worsened. male. Twenty patients were excluded because the papers Neovascular Glaucoma One patient (2.2%) had complications recorded their medical records could not be found in the of neovascular glaucoma 2mo after the onset CRAO because hospital. The control group had 225 patients, with a mean age of the ocular ischaemia. The other 44 patients (97.8%) did not of 60.01±10.14y. The follow-up time ranged from 2 to 114mo have complications of neovascular glaucoma during follow-up (mean 44.91±30.23mo) in the case group. And in control time span. group, it was 60mo (from 2010 to 2015). Twenty-eight patients Associated Systemic Abnormalities (62.2%) had CRAO, 17 patients (37.8%) had BRAO (Table 1), Comorbidity of systemic diseases Totally 33 patients (73.3%) in which 2 patients had CLRAO (Figure 1). One patient with had a comorbidity of hyperlipidaemia. Thirty patients (66.7%) CLRAO case suffered from the onset of RAO in the morning. had a comorbidity of hypertension, 18 patients (40.0%) had The length of time between the onset of the RAO attack a history of stroke, 11 patients (24.4%) had coronary disease, and admission to the hospital ranged from 2h to 1mo (mean and 10 patients (22.2%) had diabetes mellitus. Furthermore, 82.51±126.77h). other than the 18 patients who had a stroke before the onset of Visual Acuity Of the 28 CRAO patients, the initial VA RAO (mean 4.04±3.88y before the RAO), there were another evaluation at admission revealed light perception VA in 9 10 patients (22.2%) who were diagnosed with stroke based on patients (32.1%), hand motion VA in 6 patients (21.4%) and imaging while hospitalized in the RAO ward, and 3 patients counting fingers VA in 6 patients (21.4%); 7 patients (25.0%) (6.7%) had a stroke at 1, 4, and 7y, respectively, after the had a VA better than 0.01. Of the 17 BRAO patients, VA onset of RAO. There were 3 patients (6.7%) who had cancer,

433 Stroke and retinal artery occlusion

1 had lung cancer, 1 had lymphoma, and 1 had prostatic carcinoma. Carotid ultrasonography There were 36 patients (80.0%) who underwent carotid artery ultrasonography examinations in the RAO group in the time when they took therapy for the RAO in the hospital, and 32 of these patients (88.9%) had plaques in the common carotid artery. Twenty-nine patients (90.6%) had bilateral involvement of the common carotid arteries. Thirty-one patients (96.9%) had plaques in the carotid artery ipsilateral to the affected eye. There were 2 patients (6.3%) who had stenosis of approximately 63% and 80%, respectively, and all the other patients (30 cases, 93.8%) Figure 2 Carotid artery ultrasonography The plaque in the left had <50% stenosis. In the common carotid artery, 7 patients internal carotid artery (yellow arrow). (21.9%) had hypoechoic plaques only, 9 patients (28.1%) had hyperechoic plaques only, and 16 patients (50.0%) had plaques with mixed echogenicity. Three patients (8.3%) had plaques in the internal carotid artery (Figure 2). The 3 internal carotid artery plaques were all hypoechoic plaques (Table 2). Forty- three cases in the RAO group took the examination in 2010 Kailuan study. Twenty-three cases (51.1%) had plaques in the carotid artery. All the people in the control group took the examination in 2010 Kailuan study. And 163 cases (72.4%) had plaques in the carotid artery. Transthoracic echocardiography was performed in 28 patients (62.2%). Nine patients (32.1%) had abnormal findings that manifested as valvular insufficiency and valvular regurgitation. A single valve or multiple valves were involved. The mitral valve was involved in 8 patients (88.9%). The aortic valve was involved in 4 patients (44.4%). Figure 3 Cranial CT scan Malacia in the basal ganglia (black arrow). The tricuspid valve was involved in 3 patients (33.3%). Three Table 2 The carotid artery ultrasonography n (%) patients had an , and all of them manifested as The common The internal Variable bradyarrhythmia. carotid carotid Cranial computed tomography scan A cranial CT scan Took examination 36 (80.0) 36 (80.0) was performed in 38 patients (84.4%), in which 31 patients Normal 4 (11.1) 33 (91.7) (81.6%) had infarctions or malacia, and the lesions were single Abnormal 32 (88.9) 3 (8.3) or multiple. The basal ganglia and centrum semiovale were Bilateral 29 (90.6) 0 the most frequently involved regions (Figure 3). Twenty-two Ipsilateral with the sick eye 31 (96.9) 2 (66.7) patients (71.0%) had a lesion ipsilateral to the affected eye Stenosis <50% 30 (93.8) 3 (100) (Table 3). Stenosis ≥50% 2 (6.3) 0 Statistical Analysis of Risk Factors The major demographic and clinical features of the two group was showed in Table 4, which Table 3 The cranial CT scan included the demographic information, lifestyle, comorbidities Variable Cases (%) and systemic diseases of the patients and other major basic Took examination 38 (84.4) data. In the univariable logistic regression analysis showed that Normal 7 (18.4) smoking (P=0.007, OR=2.368, 95%CI: 1.270-4.415), stroke Abnormal 31 (81.6) (P<0.001, OR=23.427, 95%CI: 12.754-43.035), and systolic Ipsilateral with the sick eye 22 (71.0) pressure (P=0.001, OR=1.020, 95%CI: 1.008-1.032) had The basal ganglia involved 27 (87.1) significant difference. With the conditional multivariate logistic Semioval involved 7 (22.6) regression analysis, RAO was found to be associated with Ventriculus lateralis involved 5 (16.1)

434 Int J Ophthalmol, Vol. 13, No. 3, Mar.18, 2020 www.ijo.cn Tel: 8629-82245172 8629-82210956 Email: [email protected]

Table 4 The major demographic and clinical features of RAO group and control group n (%) Variable The RAO group (n=45) The control group (n=225) Total (n=270) P Male 36 (80.0) 195 (86.7) 231 (85.6) 0.809 Age (y) 59.98±10.26 60.01±10.14 60.01±10.14 0.985 BMI (kg/m2) 25.25±3.66 24.48±2.71 24.60±2.90 0.107 HR (min) 72.64±7.98 72.39±11.67 72.43±11.16 0.894 SBP (mm Hg) 141.37±19.96 134.18±20.89 135.37±20.87 0.035 DBP (mm Hg) 84.64±11.54 82.78±10.77 83.09±10.90 0.296 FPG (mmol/L) 5.85±2.92 5.35±1.34 5.44±1.71 0.078 TG (mmol/L) 1.48±0.93 1.61±1.26 1.59±1.21 0.540 TC (mmol/L) 5.13±0.90 4.77±0.89 4.83±0.90 0.105 Carotid plaque 23 (51.1)a 163 (72.4) 186 (68.9) 0.008 Smoking 25 (55.6) 84 (37.3) 109 (40.4) 0.030 Drinking 13 (28.9) 78 (34.7) 91 (33.7) 0.494 Stroke 17 (37.8) 1 (0.4) 18 (6.7) <0.001 Myocardial infarction 3 (6.7) 3 (1.3) 6 (2.2) 0.060 Cancer 3 (6.7) 3 (1.3) 6 (2.2) 0.060 RAO: Retinal artery occlusion; BMI: Body mass index; HR: Heart rate; SBP: Systolic blood pressure; DBP: Diastolic blood pressure; FPG: Fasting plasma glucose; TG: Triglyceride; TC: Total cholesterol. aTwo cases were missed. the history of stroke (P=0.0023, OR=28.794; 95%CI: 3.322- vertebral-basilar arterial system. The main branches of the 249.586). internal carotid arterial system in the brain are the ophthalmic DISCUSSION artery, the anterior cerebral artery, the middle cerebral artery, Patients with RAO routinely describe a history of acute the anterior choroidal artery, and the posterior communicating painless catastrophic visual loss, and the final VA of 80% of artery. The ophthalmic artery is a branch of the cerebral artery patients is less than counting fingers VA[3]. Because of the poor that arises from the internal carotid artery. RAO may share prognosis of RAO, many studies focus on the risk factors for similar risk factors with cerebrovascular diseases because of RAO to provide some suggestions for prevention. their shared vascular origins[28]. The risk factors including the In this study, the VA prognosis was poor in the case group, hypertension, diabetes mellitus, body-mass index, smoking, and some patients even worsened. The length of time between alcoholism, and so on, were related with the ischemic when the patients recognized their VA loss and when they stroke[29-30]. The relationship between cholesterol and ischemic sought therapy ranged from 2h to 1mo (mean 82.51±126.77h), stroke is controversial. But still, researchers consider the which suggests that the knowledge of this emergency in the hypercholesterolemia should not be neglected in the prevention general population is very poor. of ischemic stroke[31]. Systemic Risk Factors Systemic diseases, such as hypertension, In this study, the incidence of the stroke in both the case group diabetic mellitus, and hyperlipidemia, are widely believed to and the control group were higher than the average Chinese be associated with RAO[15-18]. In addition, atrial fibrillation, people[32]. For one thing, the Tangshan city is a costal city, coronary heart disease, coronary artery bypass graft surgery, which means the people lived there take much seafood. And facial plastic surgery, Susac’s syndrome, systemic lupus another, the Kailuan general corporation is a coal mining erythaematosus, patent foramen ovale and lymphocytic company, in which most employees are male. Therefore, the leukaemia have also been reported to cause CRAO[19-27]. diet habit and lifestyle may be a factor for its high incidence in And these conditions predispose to stroke. In this study, this whole group. But there is no study focused on the stroke hyperlipidemia (33 cases, 73.3%) was the most common incidence of these people worked in the coal mining company. comorbidity, followed by hypertension (30 cases, 66.7%), In this study, 18 patients (40.0%) had a stroke before RAO which were similar to the Callizo et al[9]. The presence of these (mean 4.04±3.88y before the RAO). In addition, 10 patients systemic diseases may cause multi-systemic dysfunction, (22.2%) diagnosed with stroke based on imaging while microcirculation disorders, and changes in blood rheology, all hospitalized in the RAO ward by the cranial CT scan, which of which may indirectly increase the risk to suffer RAO. suggests that many people have unnoticed cerebral lesions The two vascular systems that form the cerebral artery include before the onset of RAO. Twenty-two patients (71.0%) the following: the internal carotid arterial system and the had lesions ipsilateral to the affected eye. The conditional

435 Stroke and retinal artery occlusion multivariate logistic regression showed that a history of stroke small sample size. The results need to be validated in larger indicates a significantly higher risk of RAO (P=0.0023, cohorts. OR=28.794; 95%CI: 3.322-249.586). Previous studies have ACKNOWLEDGEMENTS shown that RAO patients were more susceptible to stroke in Foundations: Supported by National Natural Science the first year after the onset of RAO, particularly after the first Foundation of China (No.81570891; No.81272981); the week[7,33-34]. Unlike in a prior study[7], 3 patients (6.7%) had a Beijing Municipal Administration of Hospitals’ Ascent Plan stroke at 1, 4 and 7y, respectively, after the onset of RAO in (No.DFL20150201); Beijing Natural Science Foundation this study. Therefore, stroke patients should pay close attention (No.7151003); Advanced Health Care Professionals to their visual condition, and RAO patients should also be Development Project of Beijing Municipal Health Bureau evaluated for cerebral lesions. (No.2014-2-003); Study on Individual Diagnosis and Embolic Source The carotid arteries and the heart are the Therapy Strategy for Malignant Uveal Melanoma (No.2016- main embolic sources[14]. In this study, 9 patients (32.1%) had 1-2051); Beijing Municipal Administration of Hospitals abnormal echocardiography, which manifested as valvular Clinical Medicine Development of Special Funding Support insufficiency and valvular regurgitation. There were 36 patients (No.ZYLX201307); Science & Technology Project of (80.0%) who underwent carotid artery ultrasonography Beijing Municipal Science & Technology Commission (No. examinations in the RAO group. Thirty-two patients (88.9%) Z151100001615052). had plaques in the common carotid artery, and 29 patients Conflicts of Interest: Xiao YY, None; Wei WB, None; Wang (90.6%) had bilateral involvement of the common carotid YX, None; Lu AD, None; Chen SH, None; Song L, None; arteries. In addition, plaques with mixed echogenicity were Wu SL, None. the most frequent type of plaque, which may be indicative of REFERENCES the instability of these plaques and their tendency to move 1 Ivanisević M, Karelović D. The incidence of central retinal artery to other organs. Most patients had of occlusion in the district of Split, Croatia. Ophthalmologica 2001; <50%, which was different from the findings of Rudkin et 215(3):245-246. al[35], who reported that 27% of RAO patients had moderate 2 Lorentzen SE. Occlusion of the central retinal artery. A follow-up. Acta or significant carotid artery stenosis (>50%). 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Prevalence of ideal prognosis of RAO. The main limitation in our study was the cardiovascular health and its relationship with the 4-year cardiovascular

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